Larval development of the Indo-Pacific perciform fish, Centrogenys vaigiensis (Pisces: Centrogeniidae) J e f f r e y M. L e t s * & T h o m a s T r n s k i
Order of authorship alphabetical Fish Section, Division oj Vertebrate Zoology, a~M Centre.fi)r s Research, .4ustralian a,htseum, 6 College Street, Sycbze3: ,"vSW2000, Australia (*je{
[email protected]) t R e c e i v e d 6 MoO' [999: in revised f o r m 27,kdy /999; a c c e ~ t e d 3 August 1999)
Ichthyological Research '~;!'Tke Ichthyological S~mie~yofdap:m I999
Lets, J. M. and T. Trnski. 1999. Larval development of the Indo-Pacific perciform fish, Centrogenys vc~igiensis(Pisces: Centrogeniidae). IchthyoI. Res., 46(4): 413--418. Based on seven larvae from northern Australia, development of Cent,.'ogen~w vaigie,~sis---a species of uncertain phylogenetic amnities---is described for the
Abstract
first time. Identification was established from meristic and osteologicaI characters. Development is characterized by few morphological specializations and is apparently completed at a small size (ca 5 mm standard length). Larvae are deep-bodied and compressed. with very limited head spination (small spines on preopercle, subopercle, opercle and supracleithrum). Fin development takes place at about the time of notochord flexion, and is complete at about 4.3 ram, with the exception of anal spine three, which does not fully transform from a sol~ ray until after settlement. Fin spines are short, smooth and weak. Larvae are apparently limited to near-shore, shallow marine waters, and based on the size of what are apparently settlement-stage larvae, the pelagic period may be short.
Key words. - - Larvae; ontogeny; development; Centrogeniidae; Ceno'ogenys vaigiensis.
C
entrogenvs vaigiensis (Quoy & Gaimard, 1824)
is a small to moderate size (maximum size 20 cm in total length) cryptic, demersal fish tbund in lagoons and coastal waters o f the tropical Indo-west Pacific. It is distributed from Okinawa to the Philippines and the Indo-Malay archipelago, and to "Shark Bay, Western Australia, and Moreton Bay, Queensland on the Indian and Pacific Ocean coasts, respectively, of Australia (Weber and de Beaufort, t931; Mochizuki, 1984; Paxton et al., 1989). This species' superficial resemblance to a scorpaenid in external morphology and behaviour is reflected in the common name o f false scorpionfish. Centrogenyx vaigiensis was originally described as a scorpaenid, Scorpaena vaigiensis, by Quoy and Gaimard in 1824. Cuvier in Cuvier and Valenciennes (1829) noted a similarity to several serranid genera and renamed the species Centropristis scorpaenoides. The monotypic subgenus Centrogenys was erected for vaigiensis by Richardson (1842). However relationships of this species remain unclear. Most authors have placed C. vaigiensis in the Serranidae (McCulloch, 1929; Munro, 1967; Nelson, 1976; Paxton et al., 1989), although it has also been placed in the Percichthyidae (Mochizuki, 1984). However once the limits of these two formerly 'catch-all' families became clear (Gosline, 1966; Johnson, 1983, 1984), most au-
thors either considered it an incertae sedis taxon (Nelson, 1984, 1994) or placed it in a monotypic family Centrogeniidae (Eschmeyer and Bailey, t990; Moot and Gill, 1995): sometimes spelled Centrogenysidae (Johnson, 1984), There have also been suggestions o f a superficial resemblance to cirrhitids (Gosline, t966; Nelson, 1984), but recent analysis suggests absence of shared syaapomorphic characters with either serranids or cirrhitids (Shimokawa and Amaoka, 1995). We provide here the first description of larval development of Centrogenys vaigiensis based on seven larvae, all collected in the northern Great Barrier ReeffTorres Strait region. Adults are abundant in coastal collections, but larvae of this species are rare in collections.
Materials and Methods Definitions, measurements and abbreviations follow Leis and Trnski (1989). Sizes of larvae are body length, unless stated otherwise. Because the eye of some specimens appeared shrunken, both eye and orbit diameters were measured. Caudal-fin rays are principal rays: ie, those articulating with hypural and parhypural bones. Larvae were examined and mea-
414
]. M. Leis & T. Trnski
sured under a Zeiss SR dissecting microscope. Measurements are accurate to 0.05 ram, but were rounded to the nearest 0.1 ram. Illustrations were made with the aid of an adjustable drawing tube. Material Examined. - - A l l specimens are held in the Australian Museum Fish Collection. The seven specimens (2.9-5.0mm) were linked into a series based on body shape, meristics, the minimal head spination and pigment. All were collected singly within t0 km (six within 6 kin) of land over depths of 3-24 m off northeastern Australia. The 4.3 mm specimen (I.33753-004) was collected by dipnet in Torres Strait among floating Tzu'binaria and Sa~gassum algae. The other larvae were collected by towed nets (plankton, neuston or midwater trawl) off Townsville (I.24205-052 and -053, 1.24206-045, and 1.24240 008) or in Tortes Strait (l.24560-011 and 1.24558004). The larvae were fixed in buffered formalin and are preserved in 70% ethanol. One larva (5.0ram, 1.24206--045) and one adult (80ram SL: 1.24676051) were cleared and stained (Taylor and Van Dyke, 1985). Melanin is the only pigmentation included in the larval descriptions. Eight additional small adult specimens from northern Australia in Australian Museum collections were examined externally and 13 x-rayed (indicated by *) to supplement meristic data from the literature. These specimens were: IA.615; 1.7189; 1.17060-001"; I. 19243-002"; 1.25495-013"; 1.24676-005, 1.246770t4; 1.28978-003"; 1.34301-013"; 1.34144-005"; 1.34311-036; and 1.34398-020".
Results Identification. Tile larvae were identified as Centrogenys vaigiensis by a combination of characters, the most convincing of which were meristic data. Our postftexion larvae have the following: D X[II, 10-11; A iI, 6 (tst soft ray intermediate in morphology between ray and spine, and we assume this element transforms into a spine); P~13-14; P2 l, 5; C 8+8; and 25 myomeres. Counts of adult C. vaigiensis (Johnson, 1984; Mochizuki, 1984; this study) are as follows: D XII-XIV, 9 - I 1; A III, 5-6; Pj 13-14; P~ [, 5; C 8+8 (Johnson [1984] reports 7+7, apparently based on branched caudal rays +2); Vert 9-1 l + 14-
16=25-26 (most with 10+ I5, one each with 9+ 16, 11 + 14 and 10+ t6). The combination of the anal-fin and dorsal-fin meristics of the larvae is found in tile northern Great Barrier R e e f region only in C. vaigiensis and some scorpaeniform species (Washington et al., 19841). The scorpaeniforms either have more or fewer P~ rays, or more than 25 vertebrae, and all known scorpaenif'orm larvae have parietal spines (Washington et al., 1984), which are absent in the present larvae, Most perciforrn and scorpaeniform fishes have 9+8 caudal rays, not 8+8 as found in the present larvae. Finally, adult C vaigiensis have a supraneural formula of 0/2/1/1, as does the cleared and stained 5ram larva (Johnson [1984] reports 0/0+2/1/1, but this does not conform with our material). Larval development (Fig. 1, Tables 1, 2). Morphology.- Larvae are initially deep-bodied and decrease slightly in depth following notochord flexion. However, body depth at the anus increases slightly with development. Tile body is laterally compressed, with the trunk and tail strongly compressed in postflexion larvae. There are 24-25 myomeres (10-13+ t2-15). The large, triangular gut is tightly coiled with a relatively thick intestine, and reaches past midbody (54-65% BL). The gut projects below the ventral profile. The small, inconspicuous gas bladder is located at the dorsal apex of the gut. Tile head is large, with a prominent angle of the lower jaw that becomes less prominent after flexion. The convex snout is about as long as the eye diameter. The mouth is large and oblique, reaches to at least mid pupil and has a sharp maxillary process anteriorly. Small teeth are present in both jaws but may not be visible if the mouth is closed (Fig ID). The moderate eye is round. Gill membranes are free from the isthmus. Two nostrils are present in postflexion larvae. The 2.9mm larva (late preflexion) has three small spines on the outer preopercle border, one very small spine on both the inner preopercle border and subopercle, one weak opercular spine, and low smooth supraocular and supracleithral ridges. The postflexion larvae have up to six small outer preopercular spines, with the spine at the angle longest by a small margin, and some specimens have a second, small inner preopercular spine. The subopercular spine becomes longer and more promi-
Fig. 1. Larvae of Centrogen),s vaigiensis from the northern Great Barrier Reef region. A, B and D from plankton tows, A) 2.9 mm BL from Torres Strait (I.24560-011). Note pelvic-fin bud. B) 4.4 mm BL from near Townsvilte (I.33753-004). C) 4.3 mmBL dip-netted with floating algae in Tortes Strait (I.33753--004). Note incipient first anal-fin spine. D) 5.0 mm BL from near Townsville (1.24206-045). Subsequently cleared and stained.
Larvae of
Centrogcnys vaigiensis
415
J.M.
416
Leis & T. Trnski
nent by the flexion stage, but remains small. A second opercular spine and a cleithral ridge are present'in postflexion larvae. The supracleithral ridge becomes stronger, and in the 5 mm specimen, there is a very small, emergent spine. The lachrymal overlies the central portion of the maxilla. Notochord flexion takes place at a small size, beginning at about 2.8 ram, and is complete before 4.3 ram. Several caudalfin rays are ossified in the late-preflexion 2.9mm larva, and all rays are present by the completion o f flexion. Dorsal- and anal-fin antagen are present in the late pre-ftexion 2.9ram specimen. Incipient rays form by the late fexion stage, and most elements are ossified in early postflexion larvae. Both fins have iS.tll complements of elements by 4.4-4.6mm, however the third anal spine apparently transforms from a ray sometime after 5.0 ram. The fin spines are thin, flexible and no longer than the anterior soii rays. In the 5.0 mm specimen, dorsal spines I I - I V are marginally longer than the posterior spines. Pelvic-fin buds are present in the late preflexion 2.9 mm specimen. All pelvic-fin elements are present in postflexion larvae but the fins remain small. Incipient pectoral-fin rays are present in the iate-preflexion 2.9 mm larva, begin to ossify during flexion and all pectoral rays are present in postflexion larvae. While the pectoral rays are forming, the fin moves downward from a mid-lateral position to a position low on the body, just dorsal to the pelvic-fin base by about 4.3 mm. At the same time, the pectoral-fin enlarges to as much as 34% BL, and reaches past the anus. There is a small t-o moderate gap between the anus and origin of the anal fin. Scales are not present in any o f our larvae.
[email protected] Centroget%~,s vaigiensis larvae are ini-
Table 1.
tially lightly pigmented with a persistent metanophore on the ventral midline at the posterior margin of the anal fin, a metanophore on the dorsal midline at the posterior matgin o f the dorsal fin in some specimens, one or two small melanophores on the posterior margin of the hypural plates and one or two melanophores on the ventral midline of the gut. Melanophores may also develop on the midline o f the gutar membrane, on the dorsal and ventral midlines of the caudal peduncle near the end of both dorsal and anal fins, and, in some specimens, on the angle o f the lower jaw and internally at the origin of the anal fin. Most of the larvae examined were faded, and the location o f pigment may in fact be tess variable. During the postflexion stage, pigment develops on the head and anteriorly on the trunk, on the membranes between the first few dorsal-fin spines and on the pelvic fin, and the pigment on the gut spreads. In the larva dip-netted with floating seaweed (4.3 ram), and to a lesser extent in the 5.0 m m specimen, the head and anterior portion o f the trunk are heavily pigmented. Our material does not allow us to determine if this is larval pigment restricted to the pelagic stage, or incipient elements of the post-settlement juvenile pigment.
Discussion Specializations to pelagic larval life include the small size at all developmental stages~ the subopercular spine, and light pigmentation prior to settlement. Adults have preopercular, opercular and supracleithral spination, and we assume these are homologous
Selected morphometric characters ofCentrogenys vaigiensis larvae
Body length
Preanal length
Predorsal length
Head length
Pectoral length
Body Body depth (Pt) depth (A)
Orbit diameter
Eye diameter
Snout length
Anus to anal fin length
2.9
0.57
0.44
0.44
0.14
0.46
0.25
0.16
0.!1
0.14
0.04
2.8 3.5
0.59 0.65
0.38 0.34
0.33 0.44
0.t3 0.14
0.48 0.45
0.23 0.22
0.15 0.t5
0.12 0.11
0.10 0.14
0.04 0.05
4.3 4.4 4.6 5.0
0.54 0.65 0.56 0.58
0.35 0.34 0.33 0.35
0.39 0.37 0.40 0.38
0.29 0.26 0.34 --
0.39 0.43 0.40 0.39
0.31 0.29 0.30 0.35
0.13 0.14 0.14 0.14
0.11 0.I0 0.10 0.12
0.09 0.10 0.09 0.08
0.08 0.05 0.08 0.09
Body length given in mm, all other values are proportions of body length. Specimens between broken lines were undergoing notochord flexion. Body depth measured at both the level of the pectoral-fin base (P t), and at the anus (A). Measurements of the 5.0 mm specimen were taken after the specimen was cleared and stained, so sorne structures illustrated (Fig. ID) could not be measured.
Larvae of Centrogenys vaigiensis
with the spination present in these locations in the larvae. Because development is relatively unspecialized, larval morphology gives few clues as to the relationships of this enigmatic species. Unspecialized larval development is commonly encountered in taxa with brief pelagic stages (personal observations), and may be simply an independently-acquired adaptation to a short pelagic stage. Ceno'ogenys vaigiensis larvae are characterised by a deep body; small size at notochord flexion; light pigmentation; early-forming pelvic fins; a short anal fin; relatively weak head spination including short preopercular spines with only the spine at the angle moderately long; and a large mouth. Once the median fins form, meristics witl separate C, ~Jaigiensis larvae from most families. Families with similar larvae include scorpaenids, some carangine carangids, citharids, callanthiids, sciaenids and deep-bodied sparids. What are apparently settlement-stage C. vaigie~,sis resemble some postflexion scorpaenid larvae and have similar meristic values. However scorpaenids are larger at equivalent developmental events, have extensive head spination including parietal and infraorbital spines, and the pectoral fin is usually larger and pigmented. Carangine carangids usually have a supraoccipital crest and longer prcopercular spines, midtaterat trunk or tail pigment series, and they undergo notochord flexion at a larger size than C vaigiensis. Citharids have a similar body shape, but more myomeres (>30) and fin rays, much larger preopercular spines, and they lack large pectoral fins. Some callanthiids have a similar body shape but have more extensive preopercular spination, fewer dorsal-
Table 2. Selected meristic characters of Cet~trogenys vaigiensis larvae Body Length
Dorsal fin
Anal fin
Pectoral fin Myomeres
2.9
anlage
anlage
(3)
13+i2=25
2.8 3.5
anlage (XIt, 9)
ullage (7)
6 7
10+ 14=24 I 1+14=25
4.3 4.'4. 4.6 5.0
XItl, 10 XIII, 10 XIIL 10 XIII, 11
([)I, 6 II, 6* It. 6" tt, 6*
14 14 13 14
11+14=25 12+ 13=25 10+15=25 i 1+14=25
Values in parentheses represent incipient elements9 * -morphology of first soft ray intermediate between ray and spine. Vertebrae, not myomeres, were counted in the 5.0 mm specimen. Body length in mm,
417
fin spines (9), and lack large pectoral fins. Sciaenids also have deep-bodied, lightly-pigmented larvae with weak to moderate head spination and a short anal fin. However sciaenids have supraocular and supracleithrat spines after flexion, a larger gap between the anus and origin of the anal fin, and a late-forming pelvic fin. Deep-bodied sparids can be distinguished from C vaigiensis by the relatively well-developed head spination in the former, especially the longer and more numerous inner and outer preopercular spines, spines on the supraocular and supracleithrum, the late-forming pelvic fins, and meristic differences, especially tile number of anal-fin rays. There are large morphological differences between adults and larvae, although the larvae do share enlarged pectoral iins and a scorpaenid 'gestalt', or appearance, with the adults. The largest larvae lack scales and retain a moderate gap between the antis and anal fin. The smallest juveniles of C vaigiensis (30 ram) examined already have the greatly enlarged anal-fin spines and long, robust dorsal-fin spines that characterize adults9 There is no sign of these conditions in our larvae. The first dorsal-fin pterygiophore of juveniles and adults is very broad and robust, with a marked ridge along the anterior edge perhaps suggestive of fusion of two elements (also readily misinterpreted on x-rays as a second supraneural). In the 5 mm cleared and stained larva, there is a single Tshaped pterygiophore with no anterior ridge or other sign of fusion, and only the single supraneural found in adults. In juveniles and adults, the first anal-fin pterygiophore is enlarged, and nearly horizontal, with the medial end located 7-8 vertebral centra anterior to the distal end. In the larva, the pterygiophore is of 9moderate size and angled forward (although not horizontal), with only four vertebral centra from medial to distal ends. Thus, these features apparently form relatively rapidly following settlernent. We could not determine if the tooth plates of the fifth ceratobranchials are "'united into a triangular bone, but separated by a suture" (Weber and de Beaufort, 1931) in larvae as they are in adults. All larvae of C. vaigie~zsis were collected in shallow, nearshore waters, indicating larvae do not disperse far from adult habitat. Further, development of this species involves very few larval specializations, and is ]argety complete at a very small size tabout 5 ram), indicating that larvae may be pelagic for only a short time. Transformation from the pelagic larval stage to the benthic stage involves the considerable changes noted above. The 4.3 mm larva was captured in floating algae: on this basis, we speculate that this
J.M. L e i s
418
species may cease being pelagic at a small size and that settlement onto adult habitat might be indirect.
Acknowledgments.--Four of the larvae described here were provided by R. E. Hartwick and N. E. Milward, and M. A. McGrouther assisted in the capture of the 4.3 mm specimen. A. C. Gill provided information on Centrogenvs osteology. F. J. Neira commented constructively on an early draft of the manuscript. Our sincere thanks to all.
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